Abstract

The primate prefrontal cortex (PFC) is critical for executive functions including working memory, task switching and response selection. The functional organization of this area has been a matter of debate over a period of decades. Early models proposed segregation of spatial and object information represented in working memory in the dorsal and ventral PFC, respectively. Other models emphasized the integrative ability of the entire PFC depending on task demands, not necessarily tied to working memory. An anterior-posterior hierarchy of specialization has also been speculated, in which progressively more abstract information is represented more anteriorly. Here we revisit this debate, updating these arguments in light of recent evidence in non-human primate neurophysiology studies. We show that spatial selectivity is predominantly represented in the posterior aspect of the dorsal PFC, regardless of training history and task performed. Objects of different features excite both dorsal and ventral prefrontal neurons, however neurons highly specialized for feature information are located predominantly in the posterior aspect of the ventral PFC. In accordance with neuronal selectivity, spatial working memory is primarily impaired by inactivation or lesion of the dorsal PFC and object working memory by ventral inactivation or lesion. Neuronal responses are plastic depending on task training but training too has dissociable effects on ventral and dorsal PFC, with the latter appearing to be more plastic. Despite the absence of an overall topography, evidence exists for the orderly localization of stimulus information at a sub-millimeter scale, within the dimensions of a cortical column. Unresolved questions remain, regarding the existence or not of a functional map at the areal and columnar scale, and the link between behavior and neuronal activity for different prefrontal subdivisions.

Highlights

  • The functional organization of the prefrontal cortex (PFC) in humans and non-human primates has been a matter of long-standing debate (Riley and Constantinidis, 2016)

  • We discuss the anatomical organization of the PFC, the evidence for specialization of stimulus representation within the PFC, the capacity for plasticity based on task being executed, the evidence for functional specialization drawn from inactivation experiments, and the evidence for orderly representation of stimulus information within the cortical microcircuits

  • More neurons in the dorsolateral PFC responded to white square stimuli presented at varying spatial locations; a higher percentage of these neurons were selective for spatial location; and a greater spatial selectivity was observed among those neurons, compared to ventrolateral prefrontal neurons

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Summary

INTRODUCTION

The functional organization of the prefrontal cortex (PFC) in humans and non-human primates has been a matter of long-standing debate (Riley and Constantinidis, 2016). Neurophysiological studies in non-human primates in the 1990s described physiological correlates of functional specialization across the dorsal-ventral axis, proposing that the dorsolateral PFC is responsible for spatial working memory, and the ventrolateral PFC for object working memory (Wilson et al, 1993; Ó Scalaidhe et al, 1997, 1999). An anterior-posterior axis of functional specialization has been speculated, suggesting a hierarchical organization progressing towards anterior areas (Badre and D’Esposito, 2009) How such a hierarchy might intersect with a dorso-ventral specialization added to the confusion. We discuss the anatomical organization of the PFC, the evidence for specialization of stimulus representation within the PFC, the capacity for plasticity based on task being executed, the evidence for functional specialization drawn from inactivation experiments, and the evidence for orderly representation of stimulus information within the cortical microcircuits

ANATOMICAL ORGANIZATION
LOCALIZATION OF STIMULUS SELECTIVITY
Spatial Selectivity
Feature Selectivity
Plasticity of Stimulus Representations
FUNCTIONAL IMPLICATIONS OF DORSAL AND VENTRAL PREFRONTAL INACTIVATION
PREFRONTAL MICROCIRCUIT ORGANIZATION
Findings
CONCLUSIONS AND UNRESOLVED QUESTIONS
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